Rapid screening of sugar-nucleotide donor specificities of putative glycosyltransferases

Glycobiology

Volumn 27, Issue 3, 2017, Pages 206-212

  Sheikh, M Osman ^a   Halmo, Stephanie M ^a,b   Patel, Sneha ^a,b   Middleton, Dustin ^a,b   Takeuchi, Hideyuki ^a,b   Schafer, Christopher M ^c   West, Christopher M ^b   Haltiwanger, Robert S ^a,b   Avci, Fikri Y ^a,b   Moremen, Kelley W ^a,b   Wells, Lance ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b Oklahoma Medical Research Foundation ^*  (United States)

^c OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

Author keywords

Assays; Enzymology; Glycosyltransferase; Methods; Sugar nucleotide

Indexed keywords

EPIDERMAL GROWTH FACTOR; GLYCOSYLTRANSFERASE; SUGAR NUCLEOTIDE; URIDINE DIPHOSPHATE; URIDINE DIPHOSPHATE SUGAR; CARBOHYDRATE; NUCLEOTIDE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CELLULAR DISTRIBUTION; DICTYOSTELIUM DISCOIDEUM; DONOR; ENZYME ACTIVITY; ENZYME PURIFICATION; GLYCOSYLATION; HUMAN; HYDROLYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REACTION OPTIMIZATION; STOP CODON; STREPTOCOCCUS PNEUMONIAE; ANIMAL; BACTERIUM; BOVINE; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM;

ANIMALS; BACTERIA; CATTLE; GLYCOSYLTRANSFERASES; HUMANS; NUCLEOTIDES; SUBSTRATE SPECIFICITY; SUGARS;

EID: 85015973245     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cww114     Document Type: Article

References (38)

1. Barb AW, Meng L, Gao Z, Johnson RW, Moremen KW, Prestegard JH 2012. NMR characterization of immunoglobulin G Fc glycan motion on enzymatic sialylation. Biochemistry. 51:4618-4626.
2. Beckett D, Kovaleva E, Schatz PJ 1999. A minimal peptide substrate in biotin holoenzyme synthetase-catalyzed biotinylation. Protein Sci. 8:921-929.
3. Brockhausen I. 2014. Crossroads between bacterial and mammalian glycosyl-transferases. Front Immunol. 5:1-21.
4. Gerhard DS, Wagner L, Feingold EA, Shenmen CM, Grouse LH, Schuler G, Klein SL, Old S, Rasooly R, Good P et al. 2004. The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res. 14:2121-2127.
5. Gerin I, Ury B, Breloy I, Bouchet-Seraphin C, Bolsee J, Halbout M, Graff J, Vertommen D, Muccioli GG, Seta N et al. 2016. ISPD produces CDP-ribitol used by FKTN and FKRP to transfer ribitol phosphate onto alpha-dystroglycan. Nat Commun. 7
6. Heise N, Singh D, van der Wel H, Sassi SO, Johnson JM, Feasley CL, Koeller CM, Previato JO, Mendonca-Previato L, West CM. 2009. Molecular analysis of a UDP-GlcNAc: polypeptide alpha-N-acetylglucosaminyltransferase implicated in the initiation of mucin-type O-glycosylation in Trypanosoma cruzi. Glycobiology. 19:918-933.
7. Helm JS, Hu YN, Chen L, Gross B, Walker S. 2003. Identification of active-site inhibitors of MurG using a generalizable, high-throughput glycosyl-transferase screen. J Am Chem Soc. 125:11168-11169.
8. Inamori K, Hara Y, Willer T, Anderson ME, Zhu Z, Yoshida-Moriguchi T, Campbell KP 2013. Xylosyl-and glucuronyltransferase functions of LARGE in alpha-dystroglycan modification are conserved in LARGE2. Glycobiology. 23:295-302.
9. Kanagawa M, Kobayashi K, Tajiri M, Manya H, Kuga A, Yamaguchi Y, Akasaka-Manya K, Furukawa J, Mizuno M, Kawakami H et al. 2016. Identification of a post-translational modification with ribitol-phosphate and its defect in muscular dystrophy. Cell Rep. 14:2209-2223.
10. Ketcham C, Wang F, Fisher SZ, Ercan A, van der Wel H, Locke RD, Sirajud-Doulah K, Matta KL, West CM. 2004. Specificity of a soluble UDP-galactose: fucoside alpha1,3-galactosyltransferase that modifies the cytoplasmic glycoprotein Skp1 in Dictyostelium. J Biol Chem. 279: 29050-29059.
11. Lairson LL, Henrissat B, Davies GJ, Withers SG 2008. Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem. 77:521-555.
12. Leemhuis H, Dijkhuizen L. 2003. Engineering of hydrolysis reaction specificity in the transglycosylase cyclodextrin glycosyltransferase. Biocatal Biotransfor. 21:261-270.
13. Meng L, Forouhar F, Thieker D, Gao Z, Ramiah A, Moniz H, Xiang Y, Seetharaman J, Milaninia S, Su M et al. 2013. Enzymatic basis for N-glycan sialylation: structure of rat alpha2,6-sialyltransferase (ST6GAL1) reveals conserved and unique features for glycan sialylation. J Biol Chem. 288:34680-34698.
14. Nagahori N, Nishimura SI 2006. Direct and efficient monitoring of glycosyl-transferase reactions on gold colloidal nanoparticles by using mass spectrometry. Chem-Eur J. 12:6478-6485.
15. Palcic MM, Sujino K. 2001. Assays for glycosyltransferases. Trends Glycosci Glyc. 13:361-370.
16. Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS 2006. Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol. 24:79-88.
17. Pesnot T, Wagner GK 2008. Novel derivatives of UDP-glucose: concise synthesis and fluorescent properties. Org Biomol Chem. 6:2884-2891.
18. Phan J, Zdanov A, Evdokimov AG, Tropea JE, Peters HK IIIrd, Kapust RB, Li M, Wlodawer A, Waugh DS. 2002. Structural basis for the substrate specificity of tobacco etch virus protease. J Biol Chem. 277:50564-50572.
19. Praissman JL, Live DH, Wang S, Ramiah A, Chinoy ZS, Boons GJ, Moremen KW, Wells L. 2014. B4GAT1 is the priming enzyme for the LARGE-dependent functional glycosylation of alpha-dystroglycan. eLife. 3:e03943.
20. Praissman JL, Wells L. 2014. Mammalian O-mannosylation pathway: glycan structures, enzymes, and protein substrates. Biochemistry. 53:3066-3078.
21. Praissman JL, Willer T, Sheikh MO, Toi A, Chitayat D, Lin YY, Lee H, Stalnaker SH, Wang S, Prabhakar PK et al. 2016. The functional O-mannose glycan on α-dystroglycan contains a phospho-ribitol primed for matriglycan addition. eLife. 5:e14473.
22. Ramakrishnan B, Qasba PK 2002. Structure-based design of beta 1,4-galactosyltransferase I (beta 4 Gal-T1) with equally efficient N-acetylgalactosaminyltransferase activity: point mutation broadens beta 4 Gal-T1 donor specificity. J Biol Chem. 277:20833-20839.
23. Riemersma M, Froese DS, van Tol W, Engelke Udo F, Kopec J, van Scherpenzeel M, Ashikov A, Krojer T, von Delft F, Tessari M et al. 2015. Human ISPD is a cytidyltransferase required for dystroglycan O-mannosylation. Chem Biol. 22:1643-1652.
24. Schafer CM, Sheikh MO, Zhang D, West CM 2014. Novel regulation of Skp1 by the dictyostelium AgtA alpha-galactosyltransferase involves the Skp1-binding activity of Its WD40 repeat domain. J Biol Chem. 289: 9076-9088.
25. Schweizer F. 2007. Synthesis of fluorescently labelled and internally quenched UDP-Gal probes. Carbohydr Res. 342:1831-1840.
26. Sethi MK, Buettner FF, Ashikov A, Bakker H. 2013. In vitro assays of orphan glycosyltransferases and their application to identify Notch xylosyltrans-ferases. Methods Mol Biol. 1022:307-320.
27. Sheikh MO, Wells L. 2016. Preparation of low background sugar-nucleotide donors for use in the UDP-Glo™ glycosyltransferase assay. Promega Corporation, Madison, WI, USA.
28. Shi WW, Jiang YL, Zhu F, Yang YH, Shao QY, Yang HB, Ren YM, Wu H, Chen YX, Zhou CZ 2014. Structure of a novel O-linked N-acetyl-D-glucosamine (O-GlcNAc) transferase, GtfA, reveals insights into the gly-cosylation of pneumococcal serine-rich repeat adhesins. J Biol Chem. 289:20898-20907.
29. Sindhuwinata N, Munoz E, Munoz FJ, Palcic MM, Peters H, Peters T. 2010. Binding of an acceptor substrate analog enhances the enzymatic activity of human blood group B galactosyltransferase. Glycobiology. 20:718-723.
30. Takeuchi H, Fernandez-Valdivia RC, Caswell DS, Nita-Lazar A, Rana NA, Garner TP, Weldeghiorghis TK, Macnaughtan MA, Jafar-Nejad H, Haltiwanger RS 2011. Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc Natl Acad Sci USA. 108:16600-16605.
31. Vandersall-Nairn AS, Merkle RK, O'Brien K, Oeltmann TN, Moremen KW 1998. Cloning, expression, purification, and characterization of the acid a-mannosidase from Trypanosoma cruzi. Glycobiology. 8: 1183-1194.
32. Wagner GK, Pesnot T. 2010. Glycosyltransferases and their assays. ChemBioChem. 11:1939-1949.
33. Wang S, Shen DL, Lafont D, Vercoutter-Edouart AS, Mortuaire M, Shi Y, Maniti O, Girard-Egrot A, Lefebyre T, Pinto BM et al. 2014. Design of glycosyltransferase inhibitors targeting human O-GlcNAc transferase (OGT). MedChemComm. 5:1172-1178.
34. Willer T, Inamori K, Venzke D, Harvey C, Morgensen G, Hara Y, Beltran Valero de Bernabe D, Yu L, Wright KM, Campbell KP. 2014. The glucuronyltransferase B4GAT1 is required for initiation of LARGE-mediated alpha-dystroglycan functional glycosylation. eLife. 3:e0394.
35. Wu R, Zhou M, Wu H. 2010. Purification and characterization of an active N-acetylglucosaminyltransferase enzyme complex from Streptococci. Appl Environ Microbiol. 76:7966-7971.
36. Wu ZL, Ethen CM, Prather B, Machacek M, Jiang WP 2011. Universal phosphatase-coupled glycosyltransferase assay. Glycobiology. 21: 727-733.
37. Yang M, Brazier M, Edwards R, Davis BG 2005. High-throughput mass-spectrometry monitoring for multisubstrate enzymes: determining the kinetic parameters and catalytic activities of glycosyltransferases. ChemBioChem. 6:346-357.
38. Yoshida-Moriguchi T, Campbell KP 2015. Matriglycan: a novel polysaccharide that links dystroglycan to the basement membrane. Glycobiology. 25: 702-713.